Elsevier

Experimental Neurology

Volume 65, Issue 2, August 1979, Pages 326-342
Experimental Neurology

Effects of electrical stimulation of the lateral habenula on single-unit activity of raphe neurons

https://doi.org/10.1016/0014-4886(79)90102-XGet rights and content

Abstract

Recent anatomical studies with horseradish peroxidase injections into the anterior raphe have demonstrated that the nucleus raphe dorsalis in the rat receives a major afferent input from the lateral habenula (LHb). The present study examined electrophysiologically the effects of electrical stimulation of the LHb on the spontaneous activity of midbrain and anterior pontine raphe units in anesthetized rats. The results showed that: (a) LHb stimulation (1 or 10 Hz, 0.5 to 1.0 mA) suppressed the activity of most raphe units, with the effects outlasting the duration of the stimulation in some instances; the raphe cells which showed periods of suppression during LHb stimulation were both those of the classical serotonin type (N = 26), characterized by slow regular baseline firing rates, and other raphe cells (N=52) with faster baseline rates (to 60/s); (b) inhibition of unit activity was much less pronounced for non-raphe cells lateral to the midline; (c) anatomical control stimulation points dorsal to the LHb did not alter raphe unit activity; and (d) the pathway from the habenula to the raphe may involve a dorsal route. After a knife cut through the superior colliculus-central gray at the level of the interpeduncular nucleus, the effects of habenular stimulation were substantially reduced. Conversely, stimulation of the superior colliculus just posterior to the habenula (presumably containing descending fibers from the habenula) markedly suppressed raphe unit activity. In summary, the present electrophysiologic findings were consistent with the view that activation of habenular afferent fibers to the raphe exerted a major inhibitory influence on the spontaneous activity of midbrain and pontine raphe neurons. Considerably smaller effects were exerted on lateral reticular cells. A dorsal pathway may be involved in mediating the habenular effects on raphe activity.

References (40)

  • K. Sakai et al.

    Afferent connections of the nucleus raphe dorsalis in the cat as visualized by the horseradish peroxidase technique

    Brain Res.

    (1977)
  • K.G. Usunoff et al.

    The efferent connections of the head of the caudate nucleus in the cat: an experimental morphological study with special reference to a projection to the raphe nuclei

    Brain Res.

    (1974)
  • R.Y. Wang et al.

    Collateral inhibition of serotonergic neurons in the rat dorsal raphe nucleus: Pharmacological evidence

    Neuropharmacology

    (1978)
  • G.K. Aghajanian et al.

    Histochemical fluorescence of raphe neurons: selective enhancement by tryptophan

    Science

    (1971)
  • G.K. Aghajanian et al.

    Lysergic acid diethylamide: sensitive neuronal units in the midbrain raphe

    Science

    (1968)
  • G.K. Aghajanian et al.

    Action of psychotogenic drugs on single midbrain raphe neurons

    J. Pharmacol. Exp. Ther.

    (1970)
  • K. Akagi et al.

    Differential projections of the habenular nuclei

    J. Comp. Neurol.

    (1968)
  • A. Bjorklund et al.

    Peripheral sympathetic innervation and serotonin cells in the habenular region of the rat brain

    Z. Zellforsch.

    (1972)
  • A. Brodal et al.

    The raphe nuclei of the brain stem of the cat. III. Afferent connections

    J. Comp. Neurol.

    (1960)
  • A. Dahlstrom et al.

    Evidence for the existence of monoamine containing neurons in the central nervous sytem. I. Demonstration of monoamines in the cell bodies of brain stem neurons

    Acta Physiol. Scand.

    (1964)
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    This work was supported by National Science Foundation grant BNS 77–16512 and a grant from Burroughs Wellcome Co. A report of the findings was presented at the Society for Neuroscience, November 1978 in St. Louis, Missouri.

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